Hunter House is one of the finest examples of Georgian architecture from Newport's "golden age" in the mid-18th century. The house was built and decorated when Newport was a cosmopolitan city with a principle of religious tolerance that attracted Quakers, Baptists, Congregationalists and Sephardic Jews. The great mercantile families lived patrician lives, building harborfront mansions overlooking their trading ships, and entertained in grand style both in Newport and at their country seats on Aquidneck Island. They bought furniture and silver from local craftsmen and were the patrons of such important early painters as Robert Feke and Gilbert Stuart.

The north half of Hunter House was constructed between 1748 and 1754 by Jonathon Nichols, Jr., who was a prosperous merchant and colonial deputy. After the death of Nichols in 1756, the property was sold to Colonel Joseph Wanton, Jr., who was also a deputy governor of the colony and a merchant. He enlarged the house by adding a south wing and a second chimney, transforming the building into a formal Georgian mansion with a large central hall. Colonel Wanton also ordered the graining, or "spreckling," of the pine paneling in several rooms to resemble walnut and rosewood. During the American Revolution, Colonel Wanton fled from Newport due to his Loyalist sympathies. His house was used as the headquarters of Admiral de Ternay, commander of the French fleet, when French forces occupied Newport in 1780. After the war, Colonel Wanton's house was acquired by William Hunter, a U. S. Senator and President Andrew Jackson's charge d'affaires to Brazil. The Hunters sold the house in the mid 1860's, and it passed through a series of owners until the mid-1940's.

Concerned that the fine interiors of the house would be purchased and removed from the building, a preservation effort was initiated in 1945 by Mrs. George Henry Warren and a small group of supporters. They purchased the building in 1945 and transferred it to the newly formed Preservation Society of Newport County with Mrs. Warren as its first President. The Preservation Society chose to restore Hunter House to the era of Colonel Wanton (1757 to 1779). Today, the house exhibits examples of the finest achievements in the arts and crafts of 18th century Newport. The collections include furniture by the Townsend-Goddard family of craftsmen, premier cabinetmakers of the colonial era who worked in the neighborhood of Hunter House. Newport pewter and paintings by Cosmo Alexander, Gilbert Stuart and Samuel King are also on display. Hunter House is on the Register of National Historic Landmarks.